BLACK FLY CONTROL AND SUPPRESSION OF LEUCOCYTOZOONOSIS IN TURKEYS 1.2

Steve Horosko III and Raymond Noblet" Department of Entomology

Clemson University Clemson, SC 29634-0365

Abstract: A large-scale Simulium control program using a wettable powder formulation of Vectob8c~, Bacillus thuringicnsis val". israelensis de Bnrjnc. was conducted in coastal South Carolina to suppress Lcucocytozoon smith; (Lnveran and Lucet) transmission in turkeys. All pennanent streams within a 7.2 km radius of 8 commercial turkey fnrm in the Coast.al Plains were treated fit 1 to 2 wk intervals during the summer and carly foil of 19B I and 1982. LeucocytozoOTl smithi infection levels and pnrnsitemias in sentinel Bnd commercial lurke)' flocks were t.he major criteria used in cvaluuling the results.

Erratic and high levels of precipitation during 1981 prevented adequate treatment. of the streams. A more frequent. treatment schedule was maintained in 1982 resulting in substantial decreases in parasitemia and no losses or observable pathology in either the sentinel or commercial flocks. In 1982, as in previous years, infection levels were higher in ranged turkeys than in housed birds. During 1982, I... smilhi gllmctocytc levcls were much higher in housed turkel's than those observed in previous years. This reflected greater numbers of Simulium vectors entering the houses to feed; however. the reasons for this arc uncleal".

Key Words: Black ny, Simulium, Simuliidac, Bacillus t.huringie!flsis var. israelensis, Vect.obac~, turkeys, LeucocytoloOfl, Leucocytoloonosis.

J. Agric. Enlomol. 3(l): 10-24 (January 1986)

Black flies (DIPTERA: Simuliidae) include some of the most intolerable and voracious pests of man and animals and have been incriminated as vectors of several pathogenic organisms. It is estimated that over 20 million people suffer some degree of vision impairment due to the maria! nematode causing onchocerciasis which is transmitted by black flies. As vectors of the haemosporidian genus LeucocyLozoon, they also can cause serious losses among ducks, geese, chickens, and turkeys (reviewed by Barnett 1978).

In many areas of the world, control of immature Simuliidae still depends on the use of s}'llthetic organic pesticides. However, since the immature stages are aquatic, and due to concern over the unfavorable and sometimes disastrous environmental effects of certain of these pesticides in the aquatic habita~ alternate control methods are now receiving greater emphasis.

Chemical Control DDT was the fIrst practical and effective insecticide used against black flies

and control measures of the 1950's and 1960's relied primarily on this broad­spectrum pesticide (Fairchild and Barreda 1945). The use of DDT was discontinued

1 Presented in the Livestock and Poultry Entomology Symposium nt the Southenstern Brauch :\1eeting of the Entomological Society of Americn, Greenville, se, 1985.

2 Technical Contribution Number 2181. South Cnrolinll ;\b'liculturnl Experiment Stnliolls, Clemsoll. Received for publication I Murch 1985; accepted 15 September 1985.

3 Cmduale Research Assiswnt and Professor, respectively. Department of Enlolllolog)', Clemson Unh·ersity. Clemson SC 29634-0365.

10

HOROSKO and NOBLET: Simulium Control and Leucocylozoonosis Suppression 11

in many areas, however, due primarily to its adverse long-term effects on non-target organisms (NTO's). The ban on DDT accelerated the search for substitutes which were non-persistant and more selective for black fly control.

Temephos (Abate(f;) and methoxychlor emerged as the most effective substitutes and have been widely used and studied as to their effectiveness against black fly larvae and their impact on NTO's (Jamnback 1981). Even though these two chemicals are not as persistent in the environment and are less toxic to NTO's, they still pose a hazard to some stream insects and may have far· reaching negative effects on stream communities as a whole.

The resistance of certain black fly species to temephos was reported during the W.H.O. Onchocerciasis Control Program in the Ivol)' Coast (Guillet et aL 1981). This development has necessitated research on several possible chemical alternatives or supplements for simuliid control; some of which have shown promise (reviewed by Jamnback 1981; Wallace and Hynes 1975).

Biological Cont.rol The insecticide of choice is one which provides maximum lethal action against

the target species while having minimal adverse effects upon NTO's (Gaugler and Finney 1982). Biological control agents, specifically microbial agents, fulfill this criterion of specificity. These control agents are normally very safe, rarely appear to induce resistance, may be produced by using renewable raw materials and appear increasingly attractive (reviewed by Davidson and Sweeney 1983).

Three major parameters characterizing the usefulness of a prospective biocontrol agent are pathogenicity, ease of transmission, and the potential for mass production (Weiser and Undeen 1981). Field testing the available experimental black fly biocontrol agents hus been hampered due to difficulties involved in mass production. Two species of mermithid nematodes have been field tested against immature black flies. Gaugler and Molloy (1981) have shown Neoaplectan.a carpocapsae Weiser to produce mortality of black fly larvae in the field, causing death within as little as 2 - 4 h. These investigators also found no evidence of establishment or recycling of the nematode. Mesomermis {lumenaJis s.l. Welch has been tested in the field with limited success (Molloy and Jamnback 1977). All other field evaluations of biocontrol agents against black fly larvae have employed Bacillus thuringiensis var. israelensis (Gaugler and Finney 1982). Bacillus thuringicnsis VBr.

israelensis (/Jti) is the only biocontrol agent presently used against black flies which fully satisfies the above parameters of a good biological control agent. It is easily grown on artificial media, is readily ingested by black fly larvae, and produces mortality at adequately low concentrations (Weiser and Undeen 1981). This biocontrol agent was originally registered for use as a mosquito larvicide and since has been cleared for use against larval black flies. Three commercial products are currently available: Bactimos@ (Biochem Products), Teknar@ (Sandoz, Inc.), and Vecwbac" (Abbott Laborawries).

Field trials have shown that Bti is very effective against 18J\/'al black mes under diverse conditions and can be valuable as a replacement or supplement for current methods of black fly control. Field studies of the efficacy of Bli against black fly larvae in various stream habitats have been reviewed by Gaugler and Finney (1982). These and other studies ha\'e been summarized in Table 1.

One of the most attractive characteristics of Bti is its innocuousness to NTO's. No adverse effects have been demonstrated among various major groups of

. -Table 1. Summar)' of field trails using Bacillus thuringjen.si.~ var. israelensis against black fiy Illl"\tst. '" Mean percent morulityt

Principal Dosage Dischafl::e Nellresl Most distant black fly Product Exposure liters/min

species Cannulat.ion Conccntrlllion (min) X 103 sampling sampling

site:;: site:;: Stream location Reference

Simulium spp. Waler suspension 2.2 X 105 cells/ml 1 0.20 100(12) 60(100) NcwfolJlldlund Dudten and Calbo (agar slant) 1980

Simulium spp. Biochem/primary 0.5 ppm 15 1.i7 powder (R153·7B)

96(20) 11(705) New York Molloy and Jamnhack 19818

,.. >

Sinwlium spp. Baetimos- WP 3.7 ppm 15 8.60 tOO(·iOO) 76(2,000) New York Molloy and .Iamnhack " f.' 1981b

"' " Teknar-WDC 13.4 ppm 15 7.46 100(400) 100(1.000) New York l\'lolloy and Jamnback S 3

1981 b ~

Simulium uittatum t\bhott/formulated ;u ppm :15 23.90 70(312)9:1(:17) Tcnncs!lce Frommer " ,I. < ~

powder (6478-19.1) 1981 !"

Simulium (Jehruccum Teknar-WDC 1.0 X 106 spores/ml 10 0.16 100(0) 0(75) Guatemala Undeen et .1. Z ~

1981

Simulium damrlosum Teknar·WnC 1.5 ppm 10 27,420.0 100(0) 100(19,000) Ivory Coast Lacey et aJ. 1982 '" 00

5

Simulium venustum Teknar-WDC 40.0 ppm 6.80 100(20) 50(t,12fi) South Carolina Horo!iko and Noblet 1982

Simulium venustum TeknaI'-WnC 10.0 ppm 13.50 100(150) 0(1,300) New Hampshire Prismng and Burger 1984

• Adapted from Gaugler and Finney (1982). t Or pOI)ulat-ion reduction l Number of meters between the treatment and sampling site i.. given ill parentheses.

HOROSKO and NOBLET: Simulium Control and LeucocytOi~oonosis Suppression 13

aquatic invertebrates associated with black fly larvae, with the exception of certain nemalocerous Diptera (Table 2). The safety of Bti to man and other mammals has been well documented (reviewed by Gaugler and Finney 1982).

Suppression of Leucoc.ytozoon Disease Suppression of Leucocytozoonosis in turkeys has been achieved by growing them

away from black fly breeding areas, control of the Simulium vectors, growing turkeys in houses, and using medication to reduce or eliminate parasitism (Barnett 1978). Anthony and Richey (1958) treated large areas of black fly breeding habitat with DDT and reported reduced black fly populations, although L. smilhi parasitemias were still prevalent }{jssam et at (1975) in a large scale treatment program using the insecticide Abate<!;\ greatly reduced adult and larval black fly populations in the proximity of several commercial turkey farms. There was also a dramatic decrease in the level of blood parasitemia of L. smithi in sentinel turkeys compared with observations in the same area the previous year. Siccardi et aI. (1971,1974) reported that clopidol in the feed at levels of 0.025% and 0.0125% effectively reduced the parasitemia of L. smithi. Lower levels of the drug were judged ineffective.

'The development of resistance to chemical pesticides in many vector insects has demonstrated the urgent need for alternate or supplemental control methods. Biological control agents can be relatively inexpensive to use, have a good safety record, and rarely appear to induce resistance (Briese 1981).

Wi was used in a large-scale treatment program to control simuliid vectors of Leucocytozoon disease in turkeys in South Carolina (Horosko 1982). This was the first reported instance of Bti use to reduce disease transmission through control of the vector over an extended period of time. The objective of this research was to treat streams in the study ar-ea with Vectobac® \VP formulation of B. thuringiensis val'. israe/ensis during 1981 to control Sim.ulium vectors of L. smithi. It was realized that a similar control area was not available nor economically feasible. The initial objectives of the experiment were to control simuliid vectors over a large area, and evaluate L. smithi transmission in turkeys within the treatment zone over an extended period. Results of the 1981 study necessit.ated continuation of the research in 1982. Transmission levels of L. smithi in ranged versus housed turkeys were monitored during both years.

MATERIALS AND METHODS

This study was conducted during June - September 1981 and May - August 1982 in Malboro County, South Carolina. The area chosen is typical of the Coastal Plain region of the state. The study site included the area within a 7.2 km radius of the Bullard· McCune Turkey Farm (Fig. 1). The major criteria used to evaluate the control program were l) transmission levels of L. smith; in sentinel turkeys, 2) transmission levels and parasitemia in commercial ranged and housed turkeys, and 3) monitoring immature Simulium populations in streams within the study area

The two major streams flowing through the treatment area are Naked Creek and Crooked Creek (Fig. 1). The primary treatment sites were number 1 . 10 along these streams. In addition, key locations in temporary, wet·weather streams were frequently sampled throughout the study. Since these streams had flowing water only during periods of heavy rainfall, and did not sustain larval black flies, they were not routinely treated.

Table 2. Summary of trials uf>ing Bacil1w IhuringieruJi.<; var. israefcn.~;.<; against nontarget. strcam invertebratcs.-

Dosage

Product/ Exposure Stream Major invertebrate groups fonnulation Concentration (min) Results location Reference

Dipters t, F:phemeroptera, Trichopteru. Biochem/primal)' 0.2 ppm 10 • '0 adverse effect h'or)' Coast Dejou:t Lepidoptera, Odonata, Molluscs, Hinldinea powder (RI53-78) 1979

Chironomidae, F:lmidae. Ephemeroplera, Bioc:hem/primary 0.5 ppm 15 No adverse effect Ne\\' York Molloy and .Iamnback Plecoptcra, Trichoplera powder (RI5:J·78) 19813

Chironomidue. Ephemeroplera, Tricholltera Teknnr-WDC 1.5 ppm 10 No adverse effect h'or)' C08f>t Lacey el al. z p

1982

- Adapted from Gaugler and Finney (19Bt). t Exclusive of Simuliidae.

:I: 0 ;0 0 en

'" 0 0 0 0-

Z 0 OJ t""' t>J cl

~ " f 3 0 0 0

[ 0

i5. t""' ro c 0 0 0 '<.

0" N 0 0 0 0 0;;" en c '0

Fig. 1. County map showing Leucocytozoonosis suppression study area, Marlboro County, South Carolina. Treatment sites '"ro 00 00

0" 0

numbered 1·10. Additional sites frequently checked are marked with a star. BF = Bullard-McCune Farm. 0'

16 J. Agric. Enioma!. Vol. 3. ;.lo. I (1986)

The 10 treatment sites were set up at ca. 1.6 km intervals inside the treatment area. This distance between sites was used considering downstream carry of the treatment, accessibility of the individual sites, and the time factor involved in applying the treatment.

Treatments were applied at 7 - 14 d intervals during 1981 and at 7 d intervals during 1982. The stream discharge was measured at each site prior to treatment Concentration and treatment times are shown in Table 3. The WP formulation of B. thuringiensis var. israelensis, Vectobac@, was used as the inoculum throughout the experiment.

Table 3. Treatment parameters in the study employing Vectobac· for control of L. smithi vectors in Marlboro County, South Carolina.

Concentration Treatment Date mg/1 (~ppm) duration (min)

1981 6/17 - 8/3 2.0 10 8/10-9/30 1.3 15

1982 5/5 - 8/31 2.0 10

• illi serotype H-14, 2000 lntemnlionnl Aedes ucgypli toxic unitslmg (9.1 X 108 ANpouncl) ABC-GlOB-I.! WeUable Po.....der. Abbott Laboratories.

Dosages of 1.3 - 2.0 mg product per liter (= ppm) of stream water were administered from 16 liter carboys calibrated to empty in either 10 or 15 min. The suspensions were prepared on-site, hand agitated, and dripped into the stream to allow proper mixing. In monitoring population levels of immature Simuliidae, arrays of plastic streamers were placed at key locations in the two streams and checked prior to the succeeding Vectobac@ treatment. Approximate numbers of pupae and larvae on the streamers and the predominant species were recorded

Sentinel turkeys raised in the Leucocytoloon-free Clemson area were used to monitor L. smith; transmission. Every 7 - 14 d throughout the experiment, 5 - 7 young turkey hens (broad-breasted whites) were placed in the field as sentinels for ca 1 wk. These birds were maintained in a pen adjacent to a commercial range nock of ca. 5000 turkeys of the same variety. After the exposure period, each group of sentinel birds was transported back to Clemson and monitored for infeciion by thin blood smears made twice weekly for 4 wk beginning 13 d post-exposure to L. smithi vectors. These smears were air-dried, fixed with methanol, stained with Giemsa, and examined under oil immersion (l000 X) for the presence of garnerocytes. The number of gametocytes in 50 oil immersion fields was recorded.

Transmission levels in commercial ranged and housed nocks at t.he Bullard­McCune Fann also were monitored throughout the study_ Thin blood smears \l,'ere taken from 25 randomly chosen bi.rds from flocks of ca. 5000.

RESULTS AND DISCUSSION

Interpretation of the results of the treatment programs on the transmission or L. smithi in turkeys was difficult due to the large area involved (162.9 km 2) in the study, the number or streams, and the inherent complexities of the disease cycle.

HOROSKO and NOBLET: Simulium Control and Lcucocytozoonosis Suppression 17

The study conducted during 1982 was begun ca. 6 wk earlier than in 1981. The objective was to greatly reduce the black fly population during this time und suppress transmission of L. smith; which might have resulted from a spring relapse in previously infected birds or the presence of infected turkeys in the general area of the study (Alverson and Noblet 1977). We also decided to treat the streams at 7 d intervals in 1982 rather than every 7 - 14 d as during 198!.

The black fly species present during the experiment are shown in Table 4. The only L. smithi vector collected was S. slossonae as the univoltine S. congareenarum is a very carly spring species. Simulium slossonae was also the most prevalent throughout the st.udy, except for a period in lute August and September when S. decorum appeared in large numbers in some areas.

Table 4. Distribution by months of immature Simuliidae collected from streams in Marlboro County, South Carolina.

Species June July Aug Sept Oct

Simulium slossonae S. haysi S. jonesi S. decorum S. uenustwn/L'ereculldum complex S. tuberosum complex

The results of I>eriodic sampling for preimaginal black nies at representative treatment sites are given in Table 5. Counts were taken prior to applying the treatment on the dates shown, primarily to give un indication of the relat.ive numbers of black flies at the site and also to keep track of the population fluctuations occurring from week to week. At times it was impossible to sample these sites, part.icularly after a heavy rain due to streamer damage, accumulation of debris on the streamers, etc.

Site no. 5 was included in the sampling scheme in 1982 due to its location at the upstream edge of the study area. Data recorded from this location gave some idea of drift of larval black nics which may have occurred from outside the area. This may explain why the counts for this site were particularly high in comparison to the others (Table 5).

Random observations of the treatment sites at 4 to 18 h posttreatment showed that control of black nies in excess of 95% was being achieved throughout the study; at least in the vicinity of these sampling stations. On one occasion at site no. 5 on L9 June 1982, 8 L h posttreatment check was conducted, and of the 95 larvae which were alive on the sampling streamer (ca. 100 m below treatment site) prior to treating, 94 were found dead. On 29 June 1982, again at site no. 5, the streamer was removed from the water and early instal' larvae in excess of 200 were counted. The streamer was then replaced and the treatment was apl>lied. A 2.5 h posttreatment count revealed that 99% of the larvae were dead, but still attached to the streamer. Apparently, disturbing the larvae by taking them out of the water to count did not affect ingestion of inoculum and subsequent mortality. Also, on a few occasions treatments were administered during light to moderately heavy rain showers and still excellent control was achieved.

18 J. Agric. Entornol. Vol. 3. ~o. I (1986)

Table 5. Number of immature Simuliidae (larvae:pupae) present in selected Marlboro County, Sout.h Carolina, sampling sites during 1981-82.

Treatment and Sample site No. sampling date 4 5 8

/981 7/2 240:70 7/9 2:22 7/16 120:80 16:3 7/27 250:90 35:15 8/10 4:17 1:3 8/24 20:30 30:10 8/31 10:35 9/7 10:20 4:0 9/17 110:40 10:2

/982 5/26 75:40 400e:O" 25:30 6/2 27:30 25:40 6/9 45:34 95:10 70:14 6/22 17:45 300:0 10:25 6/29 11:5 200e:2 2L:0 7/7 35:7 400e:14 5: 1 7/14 160:60 250e:0 14:1 7/21 35:85 300.:40 7/29 450.:10 8/18 400:2 0:0 8/24 50:75 400:2 0:0 8/31 27:20 400:12 0:0

.. Instar of majority of lnn.'nc; c = carly.

It was possible to attain acceptable, but not complete, control of black fly larvae over the area. This may be attributed to various factors. Due to limitations in available manpower and time, it \Vas impossible to treat every section of water which could harbor black nies at any given time over such a large area. There were several places where the streams passed through swampy areas up to 50· 100 m in width which contained many small rivulets. In addition, there were numerous pools, or areas of relatively slow moving water, throughout the area which dilute the dosage, promote settling, and reduce the carry of the inoculum.

Erratic and high levels of rainfall in the study area during both seasons also inhibited adequate treatment at all of the treatment sites (Fig. 2). A nash flood during August of L98 L resulted in a missed treatment as a sufficient amount of material was not available to treat under those conditions. Stream flow was measured at this particular site and found 100% increase from that recorded 1 wk earlier. This missed treatment probably was responsible for the increase in blood parasitemia recorded among sentinel turkeys during the latter part of August 1981 (Table 6). There was also an increase in parasitemia noted among sampled ranged turkeys during this period (Table 7).

During the first week of August, 1982, the streams were not treated, and as in ] 981, this missed treatment may be correlated with the increase in parasitemia

80

1982 ~:: 60 t 111111111 1981 --•~

, !!!

~

~ ~

:;

40.. -•~

c ~

~ ~

20

Mil

:I: o o (f>'" o'", " 0.

Z o to C­

'"~

~ ~ n o

" "­§ , q

" 0.

c­

go

<! <; N

g o" •;;;.

.§(f>

..,HNE IULY lUG SIPI ~ •o· o

Fig. 2. Stream now measurements taken at treatment site No.8 (Crooked Creek) during 1981 - 82. :0

3

20 J. Agric. Entomol. Vol. 3, No. 1 (1986)

Table 6. Incidence of transmission and total mean gametocytemia in sentinel turkeys in Marlboro County, South Carolina, during 1981-1982.

Sentinel Dates turkeys No. infected/ Total mean* group No. exposed No. sentinels gametocytemia

1981 1 17·28 July 2/4 (3)t 1.8 2 27 - 4 Aug. 1/3 (4) 1.8 3 3 - 11 7/7 14.0 4 10 - 20 July 7/7 52.1 5 19·25 6/6 31.0 6 24 - 31 4/4 (2) 46.1 7 31 - 8 SepL 6/6 71.3 8 7 - 18 6/6 68.3

1982 1 7-14 July 0/6 0.0 2 14 - 21 0/5 (1) 0.0 3 21 - 29 2/6 1.1 4 29 - 10 Aug. 1/4 (2) 0.2 5 9 - 18 6/6 27.7 6 18 - 24 6/6 42.0 7 24 - 31 5/5 (I) 33.5 8 31 - 14 Sept. 6/6 29.5

• Totnl meAn gllmctocytcmlO in 50 oil irom. fields (1000 Xl for cflch group of turkcys/4 wk sampling period.

t Natural dcnth or prcdntioll.

recorded among sentinels and ranged turkeys at this time (Tables 6 and 7). It was apparent that during periods of favorable transmission conditions for the vector, maintaining a rigorous treatment schedule is imperative to keep transmission down and subsequent parasitemia levels low.

Table 6 depicts the incidence of transmission and gametocyte levels in sentinel turkeys throughout the experiment. Even though all sentinels were becoming infected near the first of August during both years, the gametocyte levels were lower in 1982, particularly during the latter part of the study.

Another criterion for assessing the effects of the treatment was the levels of parasitemia in ranged and housed turkeys. Tables 7 and 8 show the percent infection and mean gametocytemia of samples taken from birds in ranged and housed nocks through the study. There was a substantial reduction in mean gametocytemia in ranged turkeys in 1982 as compared to 1981. The blood parasitemia level of L. smithi usually can be closely correlated with the intensity of feeding by the simuliid vectors; thus, reduction of parasitemia over a long period of time should indicate a decrease in activity of the vectors (Kissam et aL 1975).

Even considering the high turnover rate experienced in ranged and housed flocks on a commercial turkey farm, one particular ranged flock was monitored for as long as 10 wk during both 1981 and 1982 (Table 7). In these 2 nocks, the percentage of infected birds started out relatively low and progressed to near 100% by the end of the 10 wk. An increase in the percentage of birds infected would be expected if the parasites were being transmitted at all considering the length of time these flocks spent in the field.

HOROSKO and NOBLET: Simulium Control and Leucoc)'lOzoonosis Suppression 21

Table 7. Incidence of transmission and mean gametocyternia in ranged turkeys in Marlboro County, South Carolina, during 1981-1982.

Date of Age of turkeys No. infected! Mean sample (weeks) No. sampled gametocytemia*

/98/ 7/17 10-1'1 14/25 5.4 7/28 12 21/25 10.6 8/3 13 19/25 16.5 8/10 14 21/25 8.4 8/19 15 22/25 6.8 8/24 16 23/25 4.8 8/31 17 25/25 32.9 9/17 20 25/25 23.0

10/13 10-1'2 21/23 19,9 10/21 11 25/25 29.8

1982 5/5 13-1'1 1/23 0.4 5/19 14 8/23 0.9 5/26 15 7/23 1.0 6/2 16 12/23 2.7 6/9 17 8/23 1.2 7/7 10-1'2 6/23 1.7 7/14 11 6/23 1.0 7/21 12 6/23 2.5 7/29 13 17/23 3.8 8/9 15 18/23 2.3 8/18 16 19/23 4.8 8/24 17 21/23 5.8 8/31 18 23/23 13.0 9/14 20 22/23 6.7

.. Mean gametocytemin in 50 oil imm. fields (1000 Xl for each group of turkeys. f'1 = Flock 0, 1 10"'2 = Flock No. 2

Rearing turkeys in confinement has been one of the control measures for Leucocytozoonosis in recent. years. Simulium vectors were believed not to readily enter conventional poultry houses to feed. Data from previous years showed a low percent of infection (5 - 10%) in housed turkeys (Noblet, unpublished data). Data [rom blood samples taken from housed turkeys during investigations in 1982 corroborated these results. In sampling foul' different flocks of housed birds periodically over a period of five months (Table 8), the highest percentage of inJected turkeys recorded was 13%. Table 8 also illustrates the low level of gametocytemia recorded among these birds.

In 1981, however, when a large population of vectors apparently was present, these trends showing a low percentage of housed birds exhibiting infection were not observed. Approximately 90% of the birds in one housed nock were infected in each of the three groups of samples taken from the same housed flock over a period of 3 wit- The high parasitemias in these birds was comparable with that observed in the ranged turkeys. The reason(s) for this increased level of

22 J. Agric. Entomol. Vol. 3, No. 1 (1986)

Table 8. Incidence of transmission ~d mean gametocytemia in housed turkeys in Marlboro County, South Carolina, during 1981·1982.

Date of Age of turkeys No. infected! Mean sample (weeks) No. sampled gametocytemia·

/98/ 9/7 6 2/25 0.3 9/30 18 13/25 15.1 9/30 8 21/25 23.3

10/13 10 21/25 29.2 10/21 11 23/25 38.1

/982 5/5 13 0/23 0.0 5/19 4 0/23 0.0 6/22 8 1/23 0.1 6/22 8 1/23 0.1 6/29 9 2/23 0.2 6/29 9 1/23 0.1 7/7 10 1/23 0.1 7/14 11 0/23 0.0 7/21 12 2/23 0.3 7/29 13 1/23 0.1 8/9 15 1/23 0.1 8/18 6 0/23 0.0 8/18 16 2/23 0.1 8/24 17 1/23 0.1 8/24 7 2/23 0.1 8/31 8 1/23 0.1 9/14 10 3/23 0.6

• Meon gamctocytcmio ill 50 oil imm. fields (1000 X) for ench group of turkeys.

transmission in housed turkeys is unclear and emphasizes the need for further study of the feeding behavior of Simulium vectors of L. smithi.

Bacillus thuringiensis var. israelensis possesses many attributes of a desirable biological control agent for Simuliidae in that it is highly effective, relatively inexpensive to produce, and safe for most nontarget species (Gaugler and Finney 1982). Further research is needed with this bacterium as a black fly control agent in areas where Leucocytozoonosis in turkeys is enzootic to increase the ability of investigators to reliably predict the level of simuliid control and Leucocytozoonosis suppression which can be expected under specific field conditions.

ACKNOWLEDGMENTS

This study was funded in part by Abbot.t Laboratories, t.he South Cnrolina Turkey Federation, and by the South Carolina AgriCllltllwl Experiment Station. Appreciation is expressed to Abbott Laboratories for providing the Vectobac@ used in this study.

HOROSl(O nnd NOBLET: Simulium Control find LcucocYlOzoonosis Suppression 23

REFERENCES CITED

Alverson, D. It, and R. NobleL L977. Spring relapse of Lcucocytozoon smithi (Sporozoa: Leucocytozoidae) in turkeys. J. Med. Entomo!. 14: 132-133.

Anthony, D. W., and D. J. Richey. 1958. Innuence of black ny control on the incidence of LeuCOcytoZOV1l disease in South Carolina turkeys. J. Econ. Entomol. 51: 845-847.

BarnetL B. D. 1978. Lcucoc)'tozOOrl disease of turkeys. World Poultry Science 33: 76-87. Briese, D. 1981. Hesistance of insect species to micobial pathogens, p. 511-545. In E. Dllvidson

[ed·l, Pathogenesis of invcrtebrate microbial diseases. Allnnhcld, Osman, Totowa, NJ. Davidson, E. W., and A. W. Sweeney. 1983. Microbial control of vectors: a decade of

progress. J. Med. Entomo!. 3: 235-247. Dejoux, C, 1979. Rechevches preliminaries concernant rnction de Bacillus lhuringiensis

L<;raelensis de Barjac sur 1a faune d'invenebres d'un cours d'eau tropical. \V.H_O. document VBC/79.721. II PI'.

Fairchild, G. 8., nnd E. A. Barreda. 1945. DDT as a larvicide against Simulium. J. Econ. Entomol. :J8: 694-699.

Frommer, 11. L., J. H. Nelson, M. P. Remington. and P. H. Gibbs. 1981. The innuence of extensive llqulltic vegetative growth on the larvicidal activit.y of Bacillus thuringicnsis vur. israelcn....is in reducing Simulium uiltatum (Diptera: Simuliidae) larvae in their natural habitat. Mosq. News 41: i07-712.

Gaugler, R, and J. R. Finney. 1982. A review of Bacillus thuringicnsis var. israelCTlsis (Serotype H-14) as a biological control agent of black nies. l\·tisc. Publ. Entomol Soc­Am. 12: 1-17.

Gaugler, H., nnd D. Molloy. 1981. Field evaluation of the entomogenous nematode, Neoaplectarl(/ carpocapsae. as a biolobrical control agent of black nies (Diptera: Simuliidae). Mosq. News ,11: 459-46'1.

Guillet, P., M. Egcnffe, M. Oucdruogo. and D. Quillevcre. 1981. Mise en evidence d'une resistance ml temephos dans Ie complexe Simulium damllosum IS. sallctipauli et S. soubrcsej en Cotc d'lvoire. (Zone du programme de lutte contre I'onchocercose dans la region du bassin de In Volta). Call. ORSTOM, Enl Med. Parasit.. 18: 291-299.

Horosko, S. m. 1982. Investigations using Bacillus lhllriTlgiell.~i.~ var. israelensis for control of black nies and suppression of leucocytozoonosis in turkeys. Master's Thesis, Clemson Universit.y, Clemson, SC.

Horosko, S. rn, and R. Noblet 1982. Efficacy of Bacillus tlluriflgieflsis vur. israelcmis for control of black ny larvae in South Carolina. J. Georgia Entomol. Soc. 4: 531-537.

Jamnback, H. 1981. The origins of black fly control programs, p. 71-73. /" M. Laird led.I, Black nics: the future for biological methods in integrated control. Academic Press, London.

Kissam, J. B.. R. Noblet, and G. I. Garris. 1975. Large scale aeriallreatment of an endemic area with Abal.e(§) granular larvicide to control black flies (Diptera: Simuliidac) and suppress /"cucocylOZOOfl smith; of turkeys. J. Med. Entomol. 12: 359-362.

Lacy, L. A., H. Escaffre. B. Phili(>I>on, A. Seketel~ and P. GuilleL 1982. Large river treatment. with Bacillus OlUri1lgictlsi... (H-14) for the control of Simulium clamnosum s.l. in the Onchocerciasis Control Programme. Tropenmed Pamsit. 33: 97-101.

Molloy, D., nnd H_ Jamnback. 1977. A larval black fly control field trial using mermithid parasites and its cost implications. Mosq. News 37: 104-108.

Molloy, D., and H. Jamnback. 1981a Field evaluation of Bacillus thuringicnsis \'ar. israelensis as a black ny biocontrol agent and its effects on non-target stream insects. J. Econ. Entomol 74: 314-418.

Molloy, D., and H. Jamnback. 1981 b. Screening and evaluation or Bacillus sphaericus and B. thuri1lgic1ISL<; serotype H-14 as hlock fly control agent& Annu. Rep. to \V.H.O. 25 Pl'.

Pristrang, L. A., and J. F. Burger. 1984. Effect of Bacillus tJwrillgiensis var. israelensis on a genetically-defined population of black nies (Diptera: Simuliidae) and associat.ed insects in a montane New Hampshire stream. Can. Ent. 116: 975-981.

24 J. Agrie. Eniomol. Vol. 3. No. I (1986)

Siccardi. F. J., W. J. Dericux. and H. O. Rutherford. 1971. Pathology and prevention of Lcucocylozoofl smithi infection in turkeys. J. Amer. Vel Med Assoc. 158: 1901-1902.

Siccardi, F. J., H. O. Rutherford. and W. T. Derieux. 1974. Pathology nnd prevention of Lcucocylozoon smith; infection of turkeys. Avian Dis. 18: 21-32.

Undeen, A. H" and M. H. Colbo. 1980. The erficacy of Bacillus thuringiensis vnr. israelensis against black fly larvae (DipLers: SimuJiidae) in their natural habitat Mosq. News 40: 181-184_

Undccn, A. H.. H. Takaoka, nnd K. Hansen. 1981. A test of Bacillus thurinciensis var. israclensis de Barjne as a larvicide for Simulium ochraceum. the Central American vector of onchocerciasis. Mosq. News 41: 37-40.

Wnllnce, R. R., nnd H. B. N. Hynes. 1975. The catastrophic drift of stream insects after treatments v.rith methoxychlor (1,1,I-tricholoro-2,2-Bis (P-methoxyphenyl) ethane). Environ Poll. 8: 255-268.

Weiser, J., and A. H. Undeen. 1981. Diseases of black nics, p. 181-196. III M. Laird led.l, Blnckflies: the future for biological methods in integrated control. Academic Press, London.